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Home , Frontonasal process, Mandible, Mandibular symphysis

REVIEW ARTICLE

Illustrated Review of the and Development of the Facial Region, Part 2: Late Development of the Fetal and Changes in the Face from the Newborn to Adulthood

P.M. Som and T.P. Naidich

ABSTRACT SUMMARY: The later embryogenesis of the fetal face and the alteration in the facial structure from birth to adulthood have been reviewed. Part 3 of the review will address the molecular mechanisms that are responsible for the changes described in parts 1 and 2.

art 1 of this 3-part review primarily dealt with the early em- first make contact, each is completely covered by a homoge- Pbryologic development of the face and . Part 2 will neous epithelium. A special epithelium arises at the edge of discuss the later embryonic and fetal development of the face, and each palatal shelf, facilitating the eventual fusion of these changes in facial appearance from neonate to adulthood will be shelves. The epithelium on the nasal cavity surface of the palate reviewed. will differentiate into columnar ciliated epithelium. The epi- thelium on the oral cavity side of the palate will differentiate Formation of the Palate into stratified squamous epithelium. Between the sixth and 12th weeks, the palate is formed from 3 The 2 palatal shelves also fuse with the triangular primary pal- primordia: a midline median palatine process and paired lateral ate anteromedially to form a y-shaped fusion line. The point of palatine processes (Fig 1). In the beginning of the sixth week, fusion of the secondary palatal shelves with the is merging of the paired medial nasal processes forms the intermax- marked in the adult by the . The fusion of the 2 illary process. From this, a wedge-shaped primary anterior mes- palatal shelves also results in a lengthening of the nasal cavity and enchymal mass extends posteriorly, between the internal surfaces carries the posterior choana back toward the . Ossifica- of the developing maxillae, to form the primary palate (Fig 1B). tion gradually occurs in the primary palate and then extends into The primary palate then gives rise to the premaxilla, the anterior the palatal processes to form the . The posterior por- median portion of the that encloses the 4 upper . tions of the palatal processes do not ossify. Rather they extend The is the primordium of the remaining hard posteriorly to the nasal septum and fuse to form the soft palate ad and the soft palates. Later in the sixth week, paired lateral palatine midline uvula.1,2 processes arise as medial mesenchymal projections from each maxillary process (Figs 1 and 2). Initially these grow inferiorly, Nasal Septum between the developing and the developing alveolus (see The nasal septum develops downward and posteriorly from the the sections on the and teeth) (Fig 2A). However, as the internally merged medial nasal processes and the frontonasal pro- maxilla and mandible elongate, the tongue is pulled downward cess. Fusion between the nasal septum and the palatal processes away from the lateral palatal processes. During the seventh and starts anteriorly during the ninth week and is completed by the eighth weeks (Fig 2B), the palatal shelves elevate into a hori- 12th week (Fig 2).1,2 zontal position above the tongue (Fig 2C,-D). This change in orientation is facilitated by the release of hyaluronic acid by the Mandible mesenchyme of each palatal process. When the palatal shelves During the fourth-to-fifth weeks, the mandibular processes gradually enlarge and merge in the midline. Between the fifth From the Department of Radiology, Mount Sinai School of Medicine, New York and eighth weeks, neural crest cells of the first University, New York, New York. give rise to left and right cartilaginous rods called the Meckel Please address correspondence to Peter M. Som, MD, Department of Radiology, . These form the cores around which the membra- The Mount Sinai Hospital, One Gustave Levy Place, New York, NY 10029; e-mail: [email protected] nous of the lower develops. The mandibular pro- Indicates open access to non-subscribers at www.ajnr.org cesses form the lower , the lower jaw, and the lower http://dx.doi.org/10.3174/ajnr.A3414 regions. The mentum marks the site where the 2 mandibular

10 Som Jan 2014 www.ajnr.org FIG 1. Drawings from below show the development of the palate from 6 to 7 weeks (A), 7 to 8 weeks (B), and 8 to 10 weeks (C). The lateral palatine processes grow medially and eventually merge in the midline and with the intermaxillary segment (primitive palate). The incisive canal marks the junction of the primitive and secondary palates. (Modified with permission from Levine HL, Clemente MP, eds. Chapter 1, Surgical of the Paranasal Sinus. China: 2005. Sinus Endoscopic and Microscopic Approaches. Figures 1–3. Thieme Medical Publishers Inc., Georg Thieme Verlag Stuttgart).

FIG 2. Serial frontal diagrams (A–D) from approximately 6–10 fetal weeks shown just posterior to the intermaxillary segment illustrate the progressive development of the secondary palate and its fusion with the nasal septum. processes merge in the midline. A partial or incomplete merger gingivae (Fig 3A). A small midline remnant of the labiogingival of these mandibular processes forms the common midline lamina persists as the frenulum of the upper lip (Fig 3B). dimple or cleft. Shortly after in the sixth week, a second lamina, the dental Gingiva, , and Teeth lamina, arises in the more buccal margin of the developing Until the end of the sixth week, the primordial comprise gingiva of both jaws. The dental lamina eventually will give rise only masses of mesenchymal tissue with no differentiation of to 10 spherical buds that penetrate the mesenchyme of the lips and gingivae. At the end of the sixth week, a curvilinear both jaws. The tooth buds first appear in the anterior mandible thickening of ectoderm, the labiogingival lamina, grows into followed by the anterior maxilla. Budding then continues pro- the underlying mesenchyme. Most of this lamina degenerates, gressively posteriorly to form 10 each in the creating a labiogingival groove or sulcus between the lips and maxilla and mandible. From about the 10th fetal month, deep AJNR Am J Neuroradiol 35:10–18 Jan 2014 www.ajnr.org 11 FIG 3. Drawing from above and in front (A) of the developing lips and . The labiogingival lamina develops in the common mesenchymal tissue of this region. When it dissolves, the labiogingival sulcus that remains separates the lips and gums. The dental lamina develops just behind this region and will give rise to the dental buds, which will form the deciduous and . B, Frontal photograph shows the frenulum of the upper lip, the only remaining vestige of the labiogingival lamina.

sors and arise directly from posterior extensions of the dental laminae. By the 10th week, a mesenchymal condensation called the “” invaginates into each tooth bud, resulting in the formation of a cup-shaped enamel (Fig 5A). The enamel organ has an inner epithelium, an outer epithelium, and a middle enamel reticulum (enamel pulp) (Fig 5B,-E). The dental papilla contains attenuated collections of stellate cells, which eventually give rise to most of the tooth proper, includ- ing the pulp cavity, the , and the vasculature of the tooth. The enamel organ and dental papilla are surrounded by a mes- enchymal concentration called the “dental sac.” This sac will develop into the fibrous connective tissue (periodontal liga- ment) that attaches the roots of the teeth to the alveolar bone (Fig 5C). The inner enamel epithelium later differentiates into the ameloblasts that produce the . By the third month, the mesenchymal cells in the dental papilla adjacent to the inner enamel epithelium differentiate into odontoblasts. FIG 4. Lateral drawing of the developing teeth. Note that the perma- These produce predentin and deposit the predentin adjacent to nent teeth (blue) develop medial to the deciduous teeth. (Modified the inner enamel epithelium (Fig 5C). In the sixth month, the with permission from Frank H. Netter, Atlas of Human Anatomy, 5th Edition, Saunders Elsevier, Philadelphia, 2011, Figure 56. Netter predentin calcifies to become the dentin of the tooth. Illustrations from www.netterimages.com, ©Elsevier Inc, All rights The of the tooth refers to that part of the tooth covered reserved). by enamel and projecting above the gum line. The formation of the tooth root begins when the inner and outer enamel layers components of the dental lamina create the buds for the per- penetrate into the mesenchyme to form the epithelial root sheath manent teeth along the lingual aspects of the deciduous teeth (Hertwig epithelial root sheath) (Fig 5D). Root formation takes (Fig 4). The permanent teeth have no deciduous precur- place after the crown formation has been completed. The root 12 Som Jan 2014 www.ajnr.org FIG 5. Drawings of the progressive development of the teeth from the tooth bud stage that comes from the dental lamina to the adult tooth. (Modified from http://embryology.ch/anglais/sdigestive/gesicht05.htm and www.embryo.chronolab.com/teeth.html).

canals arise through extension and later fusion of the enveloping and eighth weeks, sheet-like collections of premyoblasts and early root sheath (Fig 5F). The inner cells of the dental sac differentiate myoblasts extend from this attenuated mesenchyme to form 5 into cementoblasts, which will produce the cementum of the laminae on each side of the face, which extend into the superficial tooth. Increasing amounts of dentin reduce the pulp cavity to the portions of the future temporal, occipital, cervical, and mandib- narrow through which the vessel and pass. The ular regions. On each side of the face, the infraorbital lamina and deciduous teeth erupt through the gingiva from 6–24 months the occipital platysma are the first laminae to appear (Fig. 6). Each 3 after birth. infraorbital lamina forms the zygomaticus major, the zygomati- cus minor, the levator labii superioris, the levator labii superioris Facial Muscles alaeque nasi, the superior part of orbicularis oris, the compressor The facial muscles start to develop between the third and eighth naris, the dilator naris, the depressor septi, the orbicularis oculi, weeks when the mesoderm of the second branchial arch starts to the frontal belly of occipitofrontalis, the corrugator supercilii, and thicken just caudal to the first branchial groove. Between the sixth the procerus muscles. Each occipital lamina forms the occipital AJNR Am J Neuroradiol 35:10–18 Jan 2014 www.ajnr.org 13 FIG 6. Sagittal drawings of the progressive development of the facial muscles from the dense mesenchyme that arises near the first branchial cleft. (Modified with permission from Gasser R. The Development of the Facial Muscles in Man. Am J Anat 1967;120:357–376).

FIG 7. Lateral drawings of a 7- to 8-week embryo (A) and an 8- to 10-week fetus (B) show that the opening of the external auditory canal remains stationary but appears to rise because the progressive elongation of the jaw creates this impression. (Modified with permission from Netter’s Atlas of Human Embryology. Edited by Cochard, L.R., PhD. 2002. Icon Learning Systems, Teterboro, New Jersey, Figure 9.27. Netter Illustrations from www.netterimages.com, ©Elsevier Inc, All rights reserved) . belly of the occipitofrontalis muscle. Each temporal lamina de- Remodeling of the Face velops into the superior auricular muscles. Each mandibular During the early fetal period, the nose is flat, the mandible appears lamina forms the mandibular part of platysma, the depressor small, and the orbits face laterally. These structures will grow into labii inferioris, the , the risorius, the depressor anguli their adult configurations as facial development is completed. As oris, the buccinator, and the levator anguli oris muscles. Mes- the brain enlarges, the cranial vault expands to each side causing enchymal cells adjacent to the first branchial cleft form the the orbits to face forward. The ostia of the external auditory canals anterior auricular muscle on each side of the face. The deep remain stationary but appear to rise because the jaw elongates and muscles form separately for the mesoderm, and these muscles grows downward (Fig 7). Early on, the extends across comprise the posterior belly of digastric, the digastric tendon, nearly the full width of the embryonic face. By the seventh-to- the stapedius, and the stylohyoid muscle on each side of the eighth weeks, differential growth of the facial elements brings the face.4 eyes and lateral portions of the maxilla and mandible to a more 14 Som Jan 2014 www.ajnr.org membrane originally attached eventually corresponds to the plane of the Waldeyer ring. The progressive depth of this ring in the postnatal period is due to the dominant differential growth of the ventral face.

Summary of Contributions The forms the , the bridge, and dorsum of the nose and the nasal . The medial nasal processes form the columella of the nose, the , the perpendicular plate of the ethmoid bone and the , the cribriform plates, and the primary palate. The lateral nasal processes form the sides and alae of the nose. The maxillary processes form the upper cheek regions and most of the upper lip, the maxilla, zygoma, and secondary palate. The mandibu- lar processes form the chin, lower lip, lower cheek regions, and the mandible (Fig 8).

Pinna of the At the beginning of the sixth week, 6 auricular mesenchymal hill- ocks appear, 3 on either side of the first branchial cleft or groove. During the seventh week, the pinna of the ear will have taken its adult shape (Fig 9).

Eyelids In the sixth week, the start to form from neural crest mesenchyme and from 2 cutaneous folds of ectoderm that FIG 8. Drawing in an anterior oblique view of the late fetal face grow over the cornea. The eyelids grow rapidly until they meet showing the contributions of the various facial processes. Green and fuse to each other in the 10th week. At this time, a persis- indicates the frontonasal process; yellow, the lateral nasal pro- tent epithelial lamina arises between the eyelids. Between the cesses; purple, the medial nasal processes; orange, the maxillary processes; and blue, the mandibular processes. 26th and 28th weeks before the eyelids reopen, eye lashes and small meibomian glands begin to differentiate from the com- frontal location. Although the expansion of the cranial vault does mon epithelial lining. make the appear smaller, it is the formation of the by progressive fusion of the maxillary with the mandibular pro- Later Facial Growth cesses at the lateral angles of the mouth that most reduces the size At birth, the has a sagittal suture system that divides the of the mouth. The coronal plane along which the oropharyngeal cranium and face into left and right halves. Anteriorly, this system

FIG 9. Lateral oblique drawings of the 6 hillocks that develop about the first branchial cleft and how they eventually form the pinna of the ear. AJNR Am J Neuroradiol 35:10–18 Jan 2014 www.ajnr.org 15 FIG 10. Frontal drawing of a neonate skull (A) shows the sagittal suture system that divides the cranium and face into 2 halves. This system is made up of the metopic suture, the internasal suture, the intermaxillary suture, and the mandibular (outlined with a black line). (Modified with permission from Sobotta: Atlas der Anatomie des Menschen. ©Elsevier GmbH, Urban & Fischer Verlag Munchen. Volume 1, Edited by Putz, R. and Pabst, R. Lippincott Williams and Wilkins, Philadelphia 2001, Figure 82). B, Frontal drawing of the body of the , the greater sphenoid wings, and the between them (black). The sagittal suture system divides to run on either side of the body of the sphenoid bone because it is separated from the greater sphenoid wings by cartilage. C, Frontal drawing of the midfacial structures at approx- imately 3 years of age. The union of the ethmoid bodies (pink) with the perpendicular plate (orange) as a result of ossification of the cribriform plates (green) makes the ethmoid bone a single bone and stabilizes the interocular and upper nasal regions. The maxilla is beige; vomer, yellow; septal cartilage, light blue. is made up of the metopic suture, the internasal suture, the is the progressive enlargement of the brain and growth of the intermaxillary suture, and the (Fig cartilage between the body and greater wings of the sphenoid 10A). Posteriorly, the sagittal suture system splits around the bone. body of the sphenoid bone, along the cartilage between the In the first year of life, the metopic suture unites, and soon after, body of the sphenoid and the greater wings of the sphenoid the mandibular symphysis unites. Then the greater sphenoid wings (Fig 10B). The sagittal system does not bisect the entire skull unite with the sphenoid body. These changes close the midline sag- 5 however because other midline structures extend from the fo- ittal suture system, and it ceases to be a growth site. ramen magnum to the nasion. These structures comprise the At approximately 3 years, of the cribriform basioccipit, basisphenoid, lesser wings of the sphenoid, the plates unites the ethmoid bodies with the perpendicular plate, creating a single ethmoid bone and stabilizing the interocular perpendicular plate of the ethmoid, and the interorbital por- and upper nasal regions (Fig 10C). It has been suggested that tion of the frontal bone.5 the progressive growth of the nasal septal cartilage “pushes” By 8–9 weeks, the initial skeleton of the face is cartilaginous the midface forward and thus contributes to the facial antero- and composed of the nasal capsule in the upper face and Meckel posterior growth.5,6 cartilage in the lower face. The chondrocranium forms the skull After the third year, separation of the maxillary bones is still base. By 12 weeks, most of the ossification centers have appeared possible, as is separation of the from the maxilla. in the membranous bones, and the enchondral ethmoid bone has However, with completion of the growth of the orbits between the started to ossify. Ossification then proceeds within these bones. seventh and 10th years, further outward movement of the maxilla During the late fetal period and until the first postnatal year, and zygoma ceases at these sutures. Further growth of the upper growth in the width of the craniofacial skeleton occurs at the facial skeleton takes place by surface bone deposition in associa- midsagittal suture system. The main mechanism of this growth tion with internal bone resorption.5 16 Som Jan 2014 www.ajnr.org FIG 11. Lateral (A) and frontal (B) drawings of neonate facial bones and skull and adult facial bones and skull in the lateral (C) and frontal (D) views. In general, the facial structures grow proportionally more and for a longer time the further they are from the neurocranium. Thus, growth of the mandible begins later and continues longer than midfacial and orbital development. The forehead grows in an anterior and slightly upward direction. The forward and upward growth of the forehead contributes to elevation and widening of the nasal bridge. (Modified with permission from Sobotta: Atlas der Anatomie des Menschen. ©Elsevier GmbH, Urban & Fischer Verlag Munchen. Volume 1, Edited by Putz, R. and Pabst, R. Lippincott Williams and Wilkins, Philadelphia 2001, Figures 66, 68, 82 and 83).

Childhood to Adulthood Facial Remodeling face, but in the older face, the supraorbital region protrudes for- As one ages from childhood to adulthood, there is a constant ward of the cheek (Fig 12). growth and remodeling of the facial bones, which results in In the transverse plane, the maxillary bones and the ethmoid changes in the facial morphology. Overall, there is forward and bodies grow apart from one another so that the interocular dis- downward growth of the face with progressing age. As a general- tance increases with age (Fig 12C). The movement of the nasal ity, the farther structures lie from the neurocranium, the longer area combined with the malar movement results in an increase in they grow and the more they increase in size. Thus, growth of the the vertical size and the width of the upper part of each nasal cavity mandible begins later and continues longer than does the growth (Fig 12D). The mandibular ramus becomes progressively deeper of the midface and orbits. in its anteroposterior dimension. The ramus also increases in ver- During the first decade of life, the forehead grows in an ante- tical dimension, accommodating the marked downward growth rior and slightly upward direction. This contributes to the eleva- of the nasomaxillary complex and the eruption of the teeth (Fig 12 tion and widening of the nasal bridge (Fig 11B,-D). The zygomatic/maxillary region grows progressively posteri- A,-C). orly as the becomes elongated by addition of new bone The young face appears somewhat brachycephalic because it is on the posterior margin of the maxilla. That part of the maxilla relatively wide and vertically short. The has not yet be- anterior to the zygomatic arch regresses while the posterior por- come fully established, and the jaws have not yet grown to their tion increases in size.6,7 full vertical extent. The young face also appears small compared The backward movement of the malar region and the forward with the cranium when the craniofacial sizes are compared growth of the supraorbital region serve to draw out the antero- with an adult skull (Fig 11). Thus, compared with an adult face, posterior dimensions of the face. The inferior orbital rim and the the young face appears “cute,” with wide-set large eyes, a small superior orbital rim are in the same coronal plane in the young jaw, a small “pug” nose, prominent cheeks, a high flat forehead AJNR Am J Neuroradiol 35:10–18 Jan 2014 www.ajnr.org 17 FIG 12. Lateral diagram of the fetal skull (A) (darker areas) and the adult skull (B) (lighter areas) shows that the inferior orbital rim and the superior orbital rim are in the same plane in the young face (dark line in A), but in the older face, the supraorbital region protrudes forward of the cheek (dark line in B). Frontal diagrams (C and D) show that as the maxillary bones and the ethmoid bodies separate from one another, this movement increases the lateral growth of the interocular distance. As a result, the orbits enlarge and shift laterally (C). The movement of the nasal area combined with the malar movement results in an increase in the vertical size and the width of the upper part of each nasal cavity (D). (Modified with permission from Enlow D. A Morphogenetic Analysis of Facial Growth. Am J Orthodontics 1966;52:283–299. Figures 1 and 4) without full ridges, a low nasal bridge, and a small 6. Scott JH. The growth of the cranio-facial skeleton. Ir J Med Sci mouth. 1962;37:276–86 7. Enlow D. A Morphogenetic analysis of facial growth. Am J Orthod 1966;52:283–99 REFERENCES 8. Levine HL, Clemente MP. Surgical anatomy of the paranasal sinus. 1. Kim CH, Park HW, Kim K, et al. Early development of the nose in In: Levine HL, Clemente MP, eds. Sinus Surgery: Endoscopic and Mi- human embryos: a stereomicroscopic and histologic analysis. La- croscopic Approaches. New York: Thieme; 2005 ryngoscope 2004;114:1791–800 9. Cochard LR, ed. Netter’s Atlas of Human Embryology. Teterboro, New 2. Warbrick JG. The early development of the nasal cavity and upper Jersey; Icon Learning Systems; 2002 lip in the human embryo. J Anat 1960;94:351–62 10. Netter FL, Craig J, Machado C. netterimages.com. Netter Illustra- 3. Abrahams JJ, Poon CS, Hayt MW. Embryology and anatomy of the tions. Elsevier. www.netterimages.com. Accessed 2011 jaw and dentition. In: Som PM, Curtin HD, eds. and 11. Human Embryology Organogenesis. 19.1. Face and upper foregut. Imaging. Philadelphia: Elsevier; 2011:1425–41 http://embryology.ch/anglais/sdigestive/gesicht05.html. Accessed 4. Gasser R. The development of the facial muscles in man. Am J Anat 2011 1967;120:357–76 12. www.embryo.chronolab.com/teeth.html. Accessed 2011 5. Scott JH. The growth in width of the facial skeleton. Am J Orthod 13. Pultz HvR, Pabst R, eds. Sobotta: Atlas der Anatomie des Menschen. 1957;43:366–71 Philadelphia: Lippincott Williams and Wilkins; 2001

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